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Land Use Change Increases Wildlife Parasite Diversity in Anamalai Hills, Western Ghats, 2 India bioRxiv preprint doi: https://doi.org/10.1101/645044; this version posted May 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Land Use Change Increases Wildlife Parasite Diversity in Anamalai Hills, Western Ghats, 2 India 3 Debapriyo Chakraborty1,2, D. Mahender Reddy1, Sunil Tiwari1, Govindhaswamy 4 Umapathy1* 5 1 CSIR-Laboratory for the Conservation of Endangered Species, Centre for Cellular and 6 Molecular Biology, Hyderabad 500048, India 7 2 Present address: EP57 P C Ghosh Road, Kolkata 700048, India 8 *[email protected] 9 10 ABSTRACT 11 Anthropogenic landscape change such as land use change and habitat fragmentation are 12 known to alter wildlife diversity. Since host and parasite diversities are strongly connected, 13 landscape changes are also likely to change wildlife parasite diversity with implication for 14 wildlife health. However, research linking anthropogenic landscape change and wildlife 15 parasite diversity is limited, especially comparing effects of land use change and habitat 16 fragmentation, which often cooccur but may affect parasite diversity substantially 17 differently. Here, we assessed how anthropogenic land use change (presence of plantation, 18 livestock foraging and human settlement) and habitat fragmentation may change the 19 gastrointestinal parasite diversity of wild mammalian host species (n=23) in Anamalai hills, 20 India. We found that presence of plantations, and potentially livestock, significantly 21 increased parasite diversity due possibly to spillover of parasites from livestock to wildlife. 22 However, effect of habitat fragmentation on parasite diversity was not significant. Together, 23 our results showed how human activities may increase wildlife parasite diversity within 24 human-dominated landscape and highlighted the complex pattern of parasite diversity 25 distribution as a result of cooccurrence of multiple anthropogenic landscape changes. 26 27 Keywords: Parasite diversity, Land use change, Plantation, Livestock, Human settlement, 28 Anamalai hills, Habitat fragmentation, Rainforest 29 1 bioRxiv preprint doi: https://doi.org/10.1101/645044; this version posted May 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 30 INTRODUCTION: 31 Land use change and habitat fragmentation are two major landscape-level outcomes of 32 human activities that significantly impact biodiversity 1–3. Consequently, considerable 33 research on biodiversity change in human-dominated landscape have been conducted, 34 which has resulted in improved understanding of how these two human impacts on 35 landscape can impact biodiversity 1,4,5. These anthropogenic factors can also modify host– 36 parasite interactions, which, in turn, can lead to either increase or decrease in parasite 37 diversity 6–8,8. Understanding how these factors may influence parasite diversity is 38 ecologically important for multiple reasons. For instance, parasites regulate host population 39 dynamics 9, alter species communities 10 and constitute a significant proportion of total 40 biomass of any ecosystem 11, which is not surprising considering parasites comprise at least 41 40% of all animal species on earth 12. Despite their ecological importance, our knowledge on 42 parasite diversity is limited13,14, particularly in the context of increasing human impact on 43 environment, underlining a significant research gap15,16. The gap is specifically wide for 44 wildlife hosts and urgent research is required in the face of recent increased emergence of 45 novel pathogens of wildlife origin 7,17,18. It is, thus, crucial to answer how anthropogenic land 46 use change and habitat fragmentation may impact parasite diversity in the wild. 47 Land use change can affect parasites both directly and indirectly. By altering 48 environment (for example, through pollution), land use change may render transmission of 49 environmentally-transmitted parasites difficult. This is particularly true for parasites that has 50 life stages outside host body. However, land use change can indirectly impact parasite 51 diversity by altering host diversity as it is one of the strongest predictors of parasite diversity 52 19–22. By decreasing host diversity and abundance, land use change can deplete richness of 53 parasites particularly those that require multiple obligatory hosts 23. This is evident when 54 many host species that are threatened in their natural habitat appear to harbour fewer 55 parasites 24. On the other hand, land use change can also increase parasite diversity in 56 multiple ways. Land use change can increase parasite diversity by increasing host diversity. 57 For instance, land use change such as agricultural field or land-fill can act as resource traps 58 and amplify host diversity artificially 25. Land use change can also increase parasite diversity 59 by introducing non-native parasites such as parasites of domestic and feral animals and 60 even from humans 26. 2 bioRxiv preprint doi: https://doi.org/10.1101/645044; this version posted May 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 61 It is also important to distinguish between different types of land use change and 62 their effects on parasites 27. One type of land use change that has not been studied well is 63 the effect of plantation on wildlife parasites 27. Plantations are usually monocultures of 64 exotic or native plant species grown as timber or fuel wood or as cash crops and have a 65 large and increasing footprint in wildlife habitats worldwide 28. They can sometime act as 66 refuge to wildlife but usually with a biotic homogenising effect29,30. Consequently, plantation 67 may also increase but homogenise parasite community. Plantations are often accompanied 68 by settlement of labourers and livestock foraging 31,32. These changes within a wildlife 69 habitat can both increase or decrease parasite diversity. Parasite diversity may decrease if 70 wildlife hosts avoid human areas to lessen confrontation with humans and resource 71 competition with livestock. On the other hand, generalist species may actually thrive in 72 human settlements by utilizing novel resources 33,34. Herbivore species may also prefer to 73 stay closer to human settlements and livestock (“spatial refugia”) that may displace 74 predators 35–38. Moreover, many wildlife, over time, may actually get habituated to humans 75 and livestock and aggregate near human-dominated landscape 39,40. These aggregations may 76 eventually increase parasite diversity by increasing contact between native host species. 77 Such situations may also increasingly expose wildlife to humans and human-associated 78 animals such as livestock and commensals, increasing chance of spillover of non-native 79 parasites to wildlife. 80 Habitat fragmentation may lead to higher parasite diversity because heavily 81 fragmented habitats may disrupt wildlife dispersal and increase host diversity in smaller 82 fragments. Such increase in host diversity in a smaller patch may alter host characteristics 83 such as home range, abundance and intra and interspecific contacts thus increasing overlap 84 among host species making host individuals exposed to higher parasite infections 41,42. 85 These effects are likely to be greatest in the smallest and most isolated of the fragments 3,43. 86 By disrupting host dispersal, fragmentations can also adversely affect parasite diversity. This 87 could be especially true for parasites who require multiple host species to complete its life 88 cycle, such as those that are transmitted trophically 44. So far, many studies looked into this 89 effect but the results have been mixed 6,41,45–47. 90 The Anamalai (Elephant hills in Tamil) hills of southern India is a highly biodiverse 91 rainforest habitat of Western Ghats, which holds about 30% of India's plant and vertebrate 3 bioRxiv preprint doi: https://doi.org/10.1101/645044; this version posted May 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 92 species diversity in less than 6% of the country’s area 48. It is also one of the most altered 93 natural habitats in India and typifies different levels of land use change and habitat 94 fragmentation rampant in Indian wildlife habitats. Large section of the habitat is highly 95 modified due to land use change, bordered by large, relatively undisturbed tropical 96 rainforests. The landscape is a matrix of over 40 rainforest fragments (1-2,500 ha in 97 size),often surrounded by plantations (coffee, tea and cardamom), roads, hydroelectric 98 dams and settlements 49. Highly-modified fragments contain within them human 99 settlements and have higher livestock pressures than other remote, less disturbed 100 fragments. In spite of such high levels of land use change and habitat fragmentation, the 101 Anamalai hills still harbour a large number of wildlife whose ranges often unavoidably 102 overlap with humans and livestock 50–53. In fact, large number of wildlife species are 103 regularly observed within human-dominated habitats and this concurrence with humans 104 often precipitates into wildlife-human conflicts 49,50,54–56. It is possible
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